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Telomeric DNA induces p53-dependent reactive oxygen species and protects against oxidative damage

  • Margaret S. Lee

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    • Tel.: +1 617 638 5500; fax: +1 617 638 5515.
    • ,
  • Mina Yaar

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    • Tel.: +1 617 638 5500; fax: +1 617 638 5515.
    • ,
  • Mark S. Eller

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    • Tel.: +1 617 638 5500; fax: +1 617 638 5515.
    • ,
  • Thomas M. Rünger

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    • Tel.: +1 617 638 5500; fax: +1 617 638 5515.
    • ,
  • Ying Gao

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    • Tel.: +1 617 638 5500; fax: +1 617 638 5515.
    • ,
  • Barbara A. Gilchrest

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    • Corresponding Author InformationCorresponding author at: Boston University School of Medicine, Department of Dermatology J-508, 609 Albany Street, Boston, MA 02118-2394, USA. Tel.: +1 617 638 5538; fax: +1 617 638 5550.

Received 22 April 2009 ,Revised 20 July 2009 ,Accepted 24 August 2009. Published online 12 July 2010 Corrected Proof

References 

  1. Moyzis RK, Buckingham JM, Cram LS, Dani M, Deaven LL, Jones MD, et al. A highly conserved repetitive DNA sequence (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci USA. 1988;85:6622–6626
  2. AS IJ, Greider CW. Short telomeres induce a DNA damage response in Saccharomyces cerevisiae. Mol Biol Cell. 2003;14:987–1001
  3. Shay JW, Wright WE. Telomeres are double-strand DNA breaks hidden from DNA damage responses. Mol Cell. 2004;14:420–421
  4. Takai H, Smogorzewska A, de Lange T. DNA damage foci at dysfunctional telomeres. Curr Biol. 2003;13:1549–1556
  5. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, et al. Extension of life-span by introduction of telomerase into normal human cells. Science (New York NY). 1998;279:349–352
  6. Hasty P, Campisi J, Hoeijmakers J, van Steeg H, Vijg J. Aging and genome maintenance: lessons from the mouse?. Science (New York NY). 2003;299:1355–1359
  7. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, et al. Mammalian telomeres end in a large duplex loop. Cell. 1999;97:503–514
  8. Karlseder J, Broccoli D, Dai Y, Hardy S, de Lange T. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science (New York NY). 1999;283:1321–1325
  9. van Steensel B, Smogorzewska A, de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell. 1998;92:401–413
  10. Eller MS, Puri N, Hadshiew IM, Venna SS, Gilchrest BA. Induction of apoptosis by telomere 3′ overhang-specific DNA. Exp Cell Res. 2002;276:185–193
  11. Ohashi N, Yaar M, Eller MS, Truzzi F, Gilchrest BA. Features that determine telomere homolog oligonucleotide-induced therapeutic DNA damage-like responses in cancer cells. J Cell Physiol. 2007;210:582–595
  12. Yaar M, Eller MS, Panova I, Kubera J, Wee LH, Cowan KH, et al. Telomeric DNA induces apoptosis and senescence of human breast carcinoma cells. Breast Cancer Res. 2007;9:R13
  13. Eller MS, Li GZ, Firoozabadi R, Puri N, Gilchrest BA. Induction of a p95/Nbs1-mediated S phase checkpoint by telomere 3′ overhang specific DNA. FASEB J. 2003;17:152–162
  14. Li GZ, Eller MS, Firoozabadi R, Gilchrest BA. Evidence that exposure of the telomere 3′ overhang sequence induces senescence. Proc Natl Acad Sci USA. 2003;100:527–531
  15. Li GZ, Eller MS, Hanna K, Gilchrest BA. Signaling pathway requirements for induction of senescence by telomere homolog oligonucleotides. Exp Cell Res. 2004;301:189–200
  16. Puri N, Eller MS, Byers HR, Dykstra S, Kubera J, Gilchrest BA. Telomere-based DNA damage responses: a new approach to melanoma. FASEB J. 2004;18:1373–1381
  17. Eller MS, Maeda T, Magnoni C, Atwal D, Gilchrest BA. Enhancement of DNA repair in human skin cells by thymidine dinucleotides: evidence for a p53-mediated mammalian SOS response. Proc Natl Acad Sci USA. 1997;94:12627–12632
  18. Goukassian DA, Eller MS, Yaar M, Gilchrest BA. Thymidine dinucleotide mimics the effect of solar simulated irradiation on p53 and p53-regulated proteins. J Invest Dermatol. 1999;112:25–31
  19. Eller MS, Liao X, Liu S, Hanna K, Backvall H, Opresko PL, et al. A role for WRN in telomere-based DNA damage responses. Proc Natl Acad Sci USA. 2006;103:15073–15078
  20. Gilchrest BA. Using DNA damage responses to prevent and treat skin cancers. J Dermatol. 2004;31:862–877
  21. Gray MD, Shen JC, Kamath-Loeb AS, Blank A, Sopher BL, Martin GM, et al. The Werner syndrome protein is a DNA helicase. Nat Genet. 1997;17:100–103
  22. Yu CE, Oshima J, Fu YH, Wijsman EM, Hisama F, Alisch R, et al. Positional cloning of the Werner's syndrome gene. Science (New York, NY). 1996;272:258–262
  23. Blander G, Kipnis J, Leal JF, Yu CE, Schellenberg GD, Oren M. Physical and functional interaction between p53 and the Werner's syndrome protein. J Biol Chem. 1999;274:29463–29469
  24. Spillare EA, Robles AI, Wang XW, Shen JC, Yu CE, Schellenberg GD, et al. p53-mediated apoptosis is attenuated in Werner syndrome cells. Genes Dev. 1999;13:1355–1360
  25. Wang XW, Tseng A, Ellis NA, Spillare EA, Linke SP, Robles AI, et al. Functional interaction of p53 and BLM DNA helicase in apoptosis. J Biol Chem. 2001;276:32948–32955
  26. Franco R, Schoneveld O, Georgakilas AG, Panayiotidis MI. Oxidative stress, DNA methylation and carcinogenesis. Cancer Lett. 2008;266:6–11
  27. Mates JM, Segura JA, Alonso FJ, Marquez J. Intracellular redox status and oxidative stress: implications for cell proliferation, apoptosis, and carcinogenesis. Arch Toxicol. 2008;82:273–299
  28. Camhi SL, Lee P, Choi AM. The oxidative stress response. vol. 3. Baltimore, MD: New horizons; 1995;p. 170–82
  29. Martindale JL, Holbrook NJ. Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol. 2002;192:1–15
  30. Thannickal VJ, Fanburg BL. Reactive oxygen species in cell signaling. Am J Physiol. 2000;279:L1005–1028
  31. Karihtala P, Soini Y. Reactive oxygen species and antioxidant mechanisms in human tissues and their relation to malignancies. Apmis. 2007;115:81–103
  32. Mates JM, Sanchez-Jimenez F. Antioxidant enzymes and their implications in pathophysiologic processes. Front Biosci. 1999;4:D339–345
  33. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39:44–84
  34. Brigelius-Flohe R. Glutathione peroxidases and redox-regulated transcription factors. Biol Chem. 2006;387:1329–1335
  35. Lei XG, Cheng WH, McClung JP. Metabolic regulation and function of glutathione peroxidase-1. Annu Rev Nutr. 2007;27:41–61
  36. Fernandes AP, Holmgren A. Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal. 2004;6:63–74
  37. Hirt RP, Muller S, Embley TM, Coombs GH. The diversity and evolution of thioredoxin reductase: new perspectives. Trends Parasitol. 2002;18:302–308
  38. Culotta VC, Yang M, O’Halloran TV. Activation of superoxide dismutases: putting the metal to the pedal. Biochim Biophys Acta. 2006;1763:747–758
  39. Johnson F, Giulivi C. Superoxide dismutases and their impact upon human health. Mol Aspects Med. 2005;26:340–352
  40. Zelko IN, Mariani TJ, Folz RJ. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med. 2002;33:337–349
  41. Kirkman HN, Gaetani GF. Mammalian catalase: a venerable enzyme with new mysteries. Trends Biochem Sci. 2007;32:44–50
  42. Leccia MT, Yaar M, Allen N, Gleason M, Gilchrest BA. Solar simulated irradiation modulates gene expression and activity of antioxidant enzymes in cultured human dermal fibroblasts. Exp Dermatol. 2001;10:272–279
  43. Toussaint O, Medrano EE, von Zglinicki T. Cellular and molecular mechanisms of stress-induced premature senescence (SIPS) of human diploid fibroblasts and melanocytes. Exp Gerontol. 2000;35:927–945
  44. Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res. 1961;25:585–621
  45. Stewart SA, Weinberg RA. Telomerase and human tumorigenesis. Semin Cancer Biol. 2000;10:399–406
  46. Sugrue MM, Shin DY, Lee SW, Aaronson SA. Wild-type p53 triggers a rapid senescence program in human tumor cells lacking functional p53. Proc Natl Acad Sci USA. 1997;94:9648–9653
  47. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell. 1997;88:593–602
  48. Zhu J, Woods D, McMahon M, Bishop JM. Senescence of human fibroblasts induced by oncogenic Raf. Genes Dev. 1998;12:2997–3007
  49. Helbock HJ, Beckman KB, Shigenaga MK, Walter PB, Woodall AA, Yeo HC, et al. DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc Natl Acad Sci USA. 1998;95:288–293
  50. von Zglinicki T. Role of oxidative stress in telomere length regulation and replicative senescence. Ann NY Acad Sci. 2000;908:99–110
  51. Freeman BA, Crapo JD. Biology of disease: free radicals and tissue injury. Lab Invest: J Tech Meth Pathol. 1982;47:412–426
  52. Babior BM. NADPH oxidase: an update. Blood. 1999;93:1464–1476
  53. Babior BM, Lambeth JD, Nauseef W. The neutrophil NADPH oxidase. Arch Biochem Biophys. 2002;397:342–344
  54. Bokoch GM, Knaus UG. NADPH oxidases: not just for leukocytes anymore!. Trends Biochem Sci. 2003;28:502–508
  55. Thannickal VJ, Aldweib KD, Fanburg BL. Tyrosine phosphorylation regulates H2O2 production in lung fibroblasts stimulated by transforming growth factor beta1. J Biol Chem. 1998;273:23611–23615
  56. Thannickal VJ. The paradox of reactive oxygen species: injury, signaling, or both?. Am J Physiol. 2003;284:L24–25
  57. Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47–95
  58. Bae YS, Kang SW, Seo MS, Baines IC, Tekle E, Chock PB, et al. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J Biol Chem. 1997;272:217–221
  59. Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science (New York, NY). 1995;270:296–299
  60. Davies KJ. The broad spectrum of responses to oxidants in proliferating cells: a new paradigm for oxidative stress. IUBMB Life. 1999;48:41–47
  61. Pryor WA, Houk KN, Foote CS, Fukuto JM, Ignarro LJ, Squadrito GL, et al. Free radical biology and medicine: it's a gas, man!. Am J Physiol Regul Integr Comp Physiol. 2006;291:R491–511
  62. Polyak K, Xia Y, Zweier JL, Kinzler KW, Vogelstein B. A model for p53-induced apoptosis. Nature. 1997;389:300–305
  63. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA. 1995;92:9363–9367
  64. Plisko A, Gilchrest BA. Growth factor responsiveness of cultured human fibroblasts declines with age. J Gerontol. 1983;38:513–518
  65. Gottlieb E, Haffner R, von Ruden T, Wagner EF, Oren M. Down-regulation of wild-type p53 activity interferes with apoptosis of IL-3-dependent hematopoietic cells following IL-3 withdrawal. EMBO J. 1994;13:1368–1374
  66. Shaulian E, Zauberman A, Ginsberg D, Oren M. Identification of a minimal transforming domain of p53: negative dominance through abrogation of sequence-specific DNA binding. Mol Cell Biol. 1992;12:5581–5592
  67. Rheinwald JG, Hahn WC, Ramsey MR, Wu JY, Guo Z, Tsao H, et al. A two-stage, p16(INK4A)- and p53-dependent keratinocyte senescence mechanism that limits replicative potential independent of telomere status. Mol Cell Biol. 2002;22:5157–5172
  68. Eller MS, Yaar M, Gilchrest BA. DNA damage and melanogenesis. Nature. 1994;372:413–414
  69. Marwaha V, Chen YH, Helms E, Arad S, Inoue H, Bord E, et al. T-oligo treatment decreases constitutive and UVB-induced COX-2 levels through p53- and NFkappaB-dependent repression of the COX-2 promoter. J Biol Chem. 2005;280:32379–32388
  70. Narayanan PK, Goodwin EH, Lehnert BE. Alpha particles initiate biological production of superoxide anions and hydrogen peroxide in human cells. Cancer Res. 1997;57:3963–3971
  71. Verdier-Sevrain S, Yaar M, Cantatore J, Traish A, Gilchrest BA. Estradiol induces proliferation of keratinocytes via a receptor mediated mechanism. FASEB J. 2004;18:1252–1254
  72. Garcia-Higuera I, Taniguchi T, Ganesan S, Meyn MS, Timmers C, Hejna J, et al. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell. 2001;7:249–262
  73. Pichierri P, Rosselli F. The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways. EMBO J. 2004;23:1178–1187
  74. Chakraborty S, Massey V. Reaction of reduced flavins and flavoproteins with diphenyliodonium chloride. J Biol Chem. 2002;277:41507–41516
  75. Cross AR, Jones OT. The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase. Biochem J. 1986;237:111–116
  76. Xie S, Wang Q, Wu H, Cogswell J, Lu L, Jhanwar-Uniyal M, et al. Reactive oxygen species-induced phosphorylation of p53 on serine 20 is mediated in part by polo-like kinase-3. J Biol Chem. 2001;276:36194–36199
  77. Shackelford RE, Innes CL, Sieber SO, Heinloth AN, Leadon SA, Paules RS. The Ataxia telangiectasia gene product is required for oxidative stress-induced G1 and G2 checkpoint function in human fibroblasts. J Biol Chem. 2001;276:21951–21959
  78. Takao N, Li Y, Yamamoto K. Protective roles for ATM in cellular response to oxidative stress. FEBS Lett. 2000;472:133–136
  79. Kinscherf R, Deigner HP, Usinger C, Pill J, Wagner M, Kamencic H, et al. Induction of mitochondrial manganese superoxide dismutase in macrophages by oxidized LDL: its relevance in atherosclerosis of humans and heritable hyperlipidemic rabbits. FASEB J. 1997;11:1317–1328
  80. Rotman G, Shiloh Y. The ATM gene and protein: possible roles in genome surveillance, checkpoint controls and cellular defence against oxidative stress. Cancer Surv. 1997;29:285–304
  81. Chen QM, Bartholomew JC, Campisi J, Acosta M, Reagan JD, Ames BN. Molecular analysis of H2O2-induced senescent-like growth arrest in normal human fibroblasts: p53 and Rb control G1 arrest but not cell replication. Biochem J. 1998;332(Pt 1):43–50
  82. Dumont P, Burton M, Chen QM, Gonos ES, Frippiat C, Mazarati JB, et al. Induction of replicative senescence biomarkers by sublethal oxidative stresses in normal human fibroblast. Free Radic Biol Med. 2000;28:361–373
  83. Reichelt J, Schachtschabel DO. Energetic stress induces premature aging of diploid human fibroblasts (Wi-38) in vitro. Arch Gerontol Geriatr. 2001;32:219–231
  84. Arad S, Konnikov N, Goukassian DA, Gilchrest BA. T-oligos augment UV-induced protective responses in human skin. FASEB J. 2006;20:1895–1897
  85. de Toledo SM, Asaad N, Venkatachalam P, Li L, Howell RW, Spitz DR, et al. Adaptive responses to low-dose/low-dose-rate gamma rays in normal human fibroblasts: the role of growth architecture and oxidative metabolism. Radiat Res. 2006;166:849–857
  86. Smith DM, Raaphorst GP. Adaptive responses in human glioma cells assessed by clonogenic survival and DNA strand break analysis. Int J Radiat Biol. 2003;79:333–339
  87. Xu Y. DNA damage: a trigger of innate immunity but a requirement for adaptive immune homeostasis. Nat Rev. 2006;6:261–270
  88. Jeeves WP, Rainbow AJ. Gamma-ray-enhanced reactivation of irradiated adenovirus in Xeroderma pigmentosum and Cockayne syndrome fibroblasts. Radiat Res. 1983;94:480–498
  89. Jeeves WP, Rainbow AJ. U.V. enhanced reactivation of U.V.-and gamma-irradiated adenovirus in normal human fibroblasts. Int J Radiat Biol Relat Stud Phys Chem Med. 1983;43:599–623
  90. Gilchrest BA, Eller MS. The tale of the telomere: implications for prevention and treatment of skin cancers J Invest Dermatol. Symposium proceedings/the Society for Investigative Dermatology, Inc. 2005;10:124–30.
  91. Preston RJ. Radiation biology: concepts for radiation protection. Health Phys. 2005;88:545–556
  92. Macip S, Igarashi M, Fang L, Chen A, Pan ZQ, Lee SW, et al. Inhibition of p21-mediated ROS accumulation can rescue p21-induced senescence. EMBO J. 2002;21:2180–2188
  93. Goukassian DA, Bagheri S, el-Keeb L, Eller MS, Gilchrest BA. DNA oligonucleotide treatment corrects the age-associated decline in DNA repair capacity. FASEB J. 2002;16:754–756
  94. Adams MM, Carpenter PB. Tying the loose ends together in DNA double strand break repair with 53BP1. Cell Div. 2006;1:19
  95. Bargonetti J, Manfredi JJ. Multiple roles of the tumor suppressor p53. Curr Opin Oncol. 2002;14:86–91
  96. Giono LE, Manfredi JJ. The p53 tumor suppressor participates in multiple cell cycle checkpoints. J Cell Physiol. 2006;209:13–20
  97. Gomez-Lazaro M, Fernandez-Gomez FJ, Jordan J. p53: twenty five years understanding the mechanism of genome protection. J Physiol Biochem. 2004;60:287–307
  98. Houtgraaf JH, Versmissen J, van der Giessen WJ. A concise review of DNA damage checkpoints and repair in mammalian cells. Cardiovasc Revasc Med. 2006;7:165–172
  99. Livneh Z. Keeping mammalian mutation load in check: regulation of the activity of error-prone DNA polymerases by p53 and p21. Cell Cycle (Georgetown Tex). 2006;5:1918–1922
  100. Loffler H, Lukas J, Bartek J, Kramer A. Structure meets function—centrosomes, genome maintenance and the DNA damage response. Exp Cell Res. 2006;312:2633–2640
  101. Lukas J, Bohr VA, Halazonetis TD. Cellular responses to DNA damage: current state of the field and review of the 52nd Benzon Symposium. DNA Repair. 2006;5:591–601
  102. Vousden KH. Activation of the p53 tumor suppressor protein. Biochim Biophys Acta. 2002;1602:47–59
  103. Hoglund P. DNA damage and tumor surveillance: one trigger for two pathways. Sci STKE. 2006;2006:pe2
  104. Roos WP, Kaina B. DNA damage-induced cell death by apoptosis. Trends Mol Med. 2006;12:440–450
  105. Yee KS, Vousden KH. Complicating the complexity of p53. Carcinogenesis. 2005;26:1317–1322
  106. Campisi J. Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell. 2005;120:513–522
  107. Thannickal VJ, Fanburg BL. Activation of an H2O2-generating NADH oxidase in human lung fibroblasts by transforming growth factor beta 1. J Biol Chem. 1995;270:30334–30338
  108. Meier B, Cross AR, Hancock JT, Kaup FJ, Jones OT. Identification of a superoxide-generating NADPH oxidase system in human fibroblasts. Biochem J. 1991;275(Pt 1):241–245
  109. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell. 2005;120:483–495
  110. Catalano A, Rodilossi S, Caprari P, Coppola V, Procopio A. 5-Lipoxygenase regulates senescence-like growth arrest by promoting ROS-dependent p53 activation. EMBO J. 2005;24:170–179
  111. Forman HJ, Torres M. Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am J Respir Crit Care Med. 2002;166:S4–8
  112. Arad S, Zattra E, Hebert J, Epstein EH, Goukassian DA, Gilchrest BA. Topical thymidine dinucleotide treatment reduces development of ultraviolet-induced basal cell carcinoma in Ptch-1±mice. Am J Pathol. 2008;172:1248–1255
  113. Goukassian DA, Helms E, van Steeg H, van Oostrom C, Bhawan J, Gilchrest BA. Topical DNA oligonucleotide therapy reduces UV-induced mutations and photocarcinogenesis in hairless mice. Proc Natl Acad Sci USA. 2004;101:3933–3938
  114. Holland PC, Clark MG, Bloxham DP, Lardy HA. Mechanism of action of the hypoglycemic agent diphenyleneiodonium. J Biol Chem. 1973;248:6050–6056
  115. Majander A, Finel M, Wikstrom M. Diphenyleneiodonium inhibits reduction of iron-sulfur clusters in the mitochondrial NADH-ubiquinone oxidoreductase (Complex I). J Biol Chem. 1994;269:21037–21042

PII: S0923-1811(09)00259-X

doi: 10.1016/j.jdermsci.2009.08.008

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